Abstract and Introduction

Abstract

We summarized studies describing the prevalence of, trends in, and correlates of nonmedical exemptions from school vaccination mandates and the association of these policies with the incidence of vaccine-preventable disease.

We searched 4 electronic databases for empirical studies published from 1997 to 2013 to capture exemption dynamics and qualitatively abstracted and synthesized the results. Findings from 42 studies suggest that exemption rates are increasing and occur in clusters; most exemptors questioned vaccine safety, although some exempted out of convenience. Easier state-level exemption procedures increase exemption rates and both individual and community disease risk.

State laws influence exemption rates, but policy implementation, exemptors' vaccination status, and underlying mechanisms of geographical clustering need to be examined further to tailor specific interventions.

Introduction

Childhood vaccinations are one of the most significant public health interventions of all time. They reduce the risk of contracting dangerous vaccine-preventable childhood diseases on the individual level and, when immunization coverage is high enough, confer herd immunity at the population level for those diseases that are contagious.[1,2] Recognizing the public health importance of the childhood immunization schedule, all 50 US states require parents to provide documentation of immunization for admission to school and day care, a mandate that has been crucial for achieving widespread vaccination.[1,2] However, all states also allow medical exemptions for those children unable to receive vaccines for medically contraindicated reasons.[3] Exemption laws in all but 2 states (Mississippi and West Virginia) also provide for nonmedical exemptions (NMEs) on the basis of parents' religious, philosophical, or personal beliefs. NMEs are considered an important mechanism to balance child welfare and the protection of public health with parental rights.[4,5] Although some have argued that NMEs should not be allowed because parents who choose not to immunize their children put their own children and others at risk,[6] others believe that the negative consequences of exemption are not sufficient to justify violating parental autonomy.

As concerns about vaccine safety have increased over the past 15 years, more parents are choosing to refuse or delay vaccines.[3,7] This increase in vaccine hesitancy can be seen at the point of school entry in the rising rates of NMEs. Furthermore, NMEs from school-entry immunization mandates are receiving increased policy and public health scrutiny because exemption rates within and across schools have significant epidemiological implications. Where NME rates are high enough to compromise herd immunity at the local level, the risk of vaccine-preventable disease outbreak increases. Understanding the spatial and social patterning of NMEs is therefore critical to infectious disease prevention and control efforts.

Over the past decade, rising attention to vaccine hesitancy and NMEs has prompted several state legislatures to introduce, consider, and in some cases enact new exemption laws. In 2003, Arkansas, which previously only allowed medical and religious exemptions, started allowing philosophical exemptions on the condition that parents provided a notarized statement requesting an exemption, completed a vaccination education component, and signed a statement acknowledging the receipt of vaccination information.[8,9] Similarly, in 2003, Texas also started to allow philosophical exemptions, requiring those who wanted to exempt to obtain a form from the Texas Department of Health and declare their objections in an affidavit.[10] Conversely, Washington, Oregon, and California, all of which previously had lenient exemption policies and, particularly in the case of Washington and Oregon, very high exemption rates, recently made the process for claiming an exemption harder by requiring a signed statement from a health care practitioner that the parent had been informed of the risks and benefits of immunization. In the 2011–2012 legislative cycle, bills to tighten or eliminate NMEs were introduced in 3 states, whereas bills to expand or allow NMEs were proposed in another 10.[11]

Continued increases in vaccine refusal and NME rates and the growing attention to NMEs in state legislatures underscore the importance of understanding the determinants of NMEs, the impact of state NME policies, and the epidemiological implications of NMEs for vaccine coverage, herd immunity, and disease outbreak risk. The goal of this systematic review, therefore, is to summarize the recent evidence on NMEs, including the prevalence of, trends in, and correlates of NMEs and the association of these exemptions and exemption policies with the incidence of vaccine-preventable disease.

All kindergarten students with nonmedical exemptions in CA and all cases of pertussis from 2005 to 2010

CA

C, E

Census tracts within a NME cluster were more likely to be in a pertussis cluster than those outside an NME cluster. Both NME and pertussis clusters were associated with high SES characteristics.

Birnbaum et al.17

2010–2011

Quantitative, cross-sectional

1018 private and public schools; kindergarteners

AZ

T, C

Rates of PBE are highly spatially aggregated in AZ and within Phoenix. Schools with highest proportion of White students had the highest PBE rates. Charter schools and those with low prevalence of free and reduced lunches had significantly higher rates of PBE.

Blank et al.11

2011–2013

Mixed, descriptive, and cross-sectional

50 states

US

S

Fourteen, 15, and 15 states were found to have easy, medium, and difficult exemption policies, respectively. States that granted philosophical exemptions and states with simpler exemption procedures had higher rates of exemption. No association was found between strictness of religious exemption policy language and percentage of children exempted for religious reasons. From 2011 to 2012, bills were introduced in 4 states restricting scope of NMEs and in 10 states broadening it. However, only bills that tightened exemption policies passed.

Britten18

2008–2009

Quantitative, cross-sectional, mathematical model

5 communities; kindergarteners

CA

T, E

Using a hypothetical population, each percentage decrease in exemption coverage was found to lead to a significant increase in severity of the outbreak and duration of the outbreak. The most significant increase in severity happened between 93% and 90% coverage, dependent on population size.

Buttenheim et al.19

2008–2010

Quantitative, cross-sectional

> 7000 private and public schools; around 500 000 kindergartners

CA

T

Crude PBE rates in CA increased 25% from 2008 to 2010, and PBE rate per 100 kindergartners increased from 1.9 to 2.3. The percentage of schools with a high PBE rate also increased from 2.2% to 2.6%. The interaction index increased from 1.6 to 2.0, and the aggregation index increased from 14.7 to 15.6, indicating increased interactions of exempted kindergarteners with other exempted kindergartners. Aggregation indexes varied widely among counties.

Centers for Disease Control and Prevention20

May–June 2005

Mixed, descriptive, cross-sectional

34 measles patients

Cincinnati, OH

E

A 17-year-old girl not vaccinated for measles contracted measles in Bucharest, Romania, during an outbreak and returned to Indiana. 34 people were later identified with measles, only 2 of whom were partially or fully vaccinated.

Centers for Disease Control and Prevention21

March 2004

Mixed, descriptive, cross-sectional

1 case of measles

Cedar Rapids, IA

E

28 students from a college with a high exemption rate went to India, and 6 measles cases occurred among the students. It was recommended they not return to the US until after the period of infectivity, but 1 student went against these precautions, alerting public health officials about the potential risk of outbreak.

Centers for Disease Control and Prevention22

March–June 2011

Mixed, descriptive, cross-sectional

2 measles outbreaks, 13 cases of measles

UT

E

Two outbreaks occurred in Utah in April and May 2011. Thirteen people were confirmed to have measles; 9 (69%) were unvaccinated and had PBEs. The infection was acquired during international travel (1 case), in households (8 cases), and schools (3 cases). Source of infection was unknown in 1 case.

Centers for Disease Control and Prevention23

April 9–July 7, 1996

Mixed, descriptive, cross-sectional

107 measles reports

Washington County, UT

E

Of the 99 measles cases who were vaccine-eligible, 64 (64%) had not been vaccinated. At the high school at which the outbreak was initially reported, 27 (3%) of 879 students were unvaccinated, and 780 (89%) had received only 1 dose of the MMR vaccine. Seventeen of the unvaccinated students had philosophic exemptions, and the other 10 had no record of measles vaccination.

Centers for Disease Control and Prevention24

January 1–April 25, 2008

Mixed, descriptive, cross-sectional

64 measles reports

NY, AZ, CA, MI, WI, HI, IL, NY, PA, VA

E

Of the 64 patients with measles 63 were unvaccinated or had unknown or undocumented vaccination status. Of these, 14 were not vaccinated because of religious or personal beliefs. 5 who had traveled abroad were unvaccinated, 2 because of personal beliefs.

Centers for Disease Control and Prevention25

January–July 2008

Mixed, descriptive, cross-sectional

131 measles reports

IL, NY, WA, AZ, CA, WI, HI, MI, AR, DC, GA, LA, MO, NM, PA, VA

E

Among the 131 measles patients, 123 were US residents, of whom 112 (91%) were unvaccinated or had unknown vaccination status. Among these 112 patients, 95 (85%) were eligible for vaccination, and 63 (66%) of those were unvaccinated because of philosophical or religious beliefs.

Centers for Disease Control and Prevention26

2009–2010

Quantitative, descriptive, cross-sectional

47 states and DC

US

T

From 2009 to 2010, total kindergarten exemption rates ranged from < 1% to 6.2% across states; 15 states had a total exemption rate ≥ 3.0%, and 15 states had exemption rates < 1%. Nonmedical exemptions ranged from 0.2% (Rhode Island) to 5.8% (Washington) among the states that allow NMEs.

Centers for Disease Control and Prevention27

2011–2012

Quantitative, descriptive, cross-sectional

49 states and DC

US

T

From 2011 to 2012, total kindergarten exemption rates ranged from < 0.1% in Mississippi to 7.0% in Alaska, with 10 reporting rates < 1%, and 9 reporting > 4% total exemption rates. The median total exemption level was 1.5%, a median increase of 0.2 percentage points compared with the 2009–2010 school year. Arkansas reported the largest increase in exemptions with an increase of 3.4 percentage points, and Nebraska reported the largest decrease, with a decrease of 2.3 percentage points. The median NME level was 1.2%, where allowed, with a range from 0.04% in Delaware and Kentucky to 5.8% in Oregon.

Centers for Disease Control and Prevention28

2012–2013

Quantitative, descriptive, cross-sectional

49 states and DC

US

T

From 2012 to 2013, the percentage of kindergarteners with an exemption was < 1% for 9 states and > 4% for 11 states, ranging from < 0.1% in Mississippi to 6.5% in Oregon, with a median of 1.8%. Georgia and West Virginia had the largest increases in total exemptions, each with an increase of 1.0 percentage point; 4 states reported decreases of > 1.0 percentage points. The median NME level was 1.5%, ranging from 0.2% in New Mexico to 6.4% in Oregon.

A significant trend of increasing vaccine coverage was found with increasing difficulty of obtaining PBE for DTP–DTaP–DT and poliovirus vaccines (P < .05) and a modest association for MMR and HepB vaccines (P < .01). Although mean vaccination coverage remains > 90% even in states in which exemptions are easy to obtain, geographic heterogeneity exists in vaccine exemptions; in Arizona, PBE rates ranged from 0.6% to 8.5% among counties, and in Washington, rates ranged from 1% to 25.3%.

Fair et al.30

1992–2000

Mixed, descriptive, cross-sectional

15 cases of tetanus in children aged < 15 y

TN, MT, MO, IN, FL, MI, CA, OH, PA, TX, WV

T, E

Fifteen cases of tetanus in children aged < 15 y were reported in 11 states. 12 (80%) children were unprotected because of lack of vaccination. Among all unvaccinated cases, objection to vaccination, either religious (n = 9) or philosophic (n = 3), was the reported reason for choosing not to vaccinate.

Feikin et al.31

1987–1998

Quantitative, time-series cohort

All children aged 3–18 y in CO

CO

S, E

The percentage of philosophical exemptions among school-aged children in Colorado increased from 1.02% to 1.87%. Exemptors were 22.2 times more likely to acquire measles and 5.9 times more likely to acquire pertussis than vaccinated children. The frequency of exemptors in a county was associated with the incidence rate of measles and pertussis in vaccinated children. Schools with pertussis outbreaks had more exemptors than schools without outbreaks. At least 11% of vaccinated children in measles outbreaks acquired infection through contact with an exemptor.

Fiebelkorn et al.32

2001–2008

Quantitative, time-series cohort

557 cases, 38 outbreaks

US

E

In the US, 557 confirmed cases of measles and 38 outbreaks were reported, 232 (42%) of which were imported from other countries. A total of 285 US-resident case-patients (65%) were considered to have preventable measles. From 2004 to 2008, a total of 68% of vaccine-eligible US-resident case-patients claimed exemptions for personal beliefs.

Gaudino & Robison33

2004–2005

Quantitative, retrospective cohort

1588 parents of OR elementary school students

OR

T, C

Exempting parents reported more markers of lower SES than nonexemptors. Exemptors were significantly more likely to have: strong vaccine concerns, > 1 childbirths at a nonhospital, distrust of local doctors, chiropractic health care, and knowledge of someone with a vaccine-hurt child, although this varied by specific communities. Exemptors were less likely to have pro-vaccine beliefs and less likely to report relying on print materials.

Gullion et al.34

Not mentioned

Qualitative, semistructured interviews

25 nonvaccinating parents

TX

C

Most (88%) of the interviewees mentioned aspects of their lifestyle that could be categorized as ''alternative living." Participants engaged in sophisticated data collection and analysis in formulating their stance on vaccinations and were skeptical of the medical community, although they placed a high value on scientific knowledge.

Gust et al.35

July and August 2003

Quantitative, cross-sectional

642 parents with at least 1 child aged < 6 y

US

C

Parents who disagreed that they had enough immunization information were more likely to report that they would not have their child immunized if it were not required by law; to believe states should grant exemptions; to mistrust the government to establish immunization policy; and to believe that they should be allowed to obtain exemptions for their child even if it raised the risk of disease for everyone else.

Gust et al.36

May 2004–February 2006

Mixed: interviews, focus groups, cross-sectional

100 cases of parents who would not immunize children if not required or who had considered filing or filed a NME and 100 controls

US

C

Parents who had filed exemptions or considered it did not differ demographically from those who did not file exemptions but were significantly more likely to have negative attitudes about immunizations, including safety, number of immunizations, and trust. A brochure intervention was found not to have improved parents' immunizations attitudes compared with controls.

Imdad et al.37

2000–2011

Quantitative, time-series cohort

All schools in NY; all pertussis cases among children aged < 19 y

NY

T, S, E

Religious exemptions in NY increased from 0.23% to 0.45% in the past 10 y, although not uniformly among counties. Counties with religious exemption prevalence rates > 1% had a higher incidence of pertussis, and a 0.1% increase in exemption rate corresponded with an increased pertussis incidence of 5 in 100 000. The mean incidence of pertussis among exempted children was 14 times that among vaccinated children. High exemption rates in a county increased pertussis risk for both vaccinated and exempted children.

Kennedy et al.38

2002

Quantitative, cross-sectional

1527 parents with at least one child aged ≤ 18 y

US

T, C, S

A parent's belief regarding compulsory vaccination for school entry is significantly associated with beliefs in the safety and utility of vaccines and the intention to have the youngest child fully vaccinated. Supportive parents were more likely to be White, to have a higher household income, and to have a smaller household size. Residence in a state that permits philosophical exemptions was also associated with a parent's opposition to compulsory vaccination.

Kennedy & Gust39

Sometime between 2005 and 2008

Mixed, focus group, interview, cross-sectional

6 church members for focus group; 12 study households involved in the outbreak for interview

IN

C

Outbreak households recognized the importance of vaccines, yet had concerns or doubts about their safety and necessity, believing that childhood vaccinations may cause serious side effects or learning disabilities. All believed in the right to refuse vaccines but were open to alternatives such as quarantine during an outbreak, and all reported that they had access to enough information on vaccination. Most said that the outbreak experience did not make their opinion of vaccines more positive.

Luthy et al.40

Not mentioned

Qualitative, cross-sectional questionnaire

287 parents

UT

C

Five overarching themes were identified regarding PBEs: parental perceptions of vaccine harm (such as the belief that vaccines caused autism), health care systems issues (insofar as filing for a PBE was more convenient), chronic disease concerns, immune system concerns, and adverse reaction concerns.

Luthy et al.41

Not mentioned

Quantitative, cross-sectional questionnaire

801 parents who have an exempted child

UT

C

The most commonly reported reason for seeking a personal exemption was vaccination conflicting with philosophical beliefs. Most parents communicated their vaccine concerns with their health care provider before seeking exemption. The majority of exempting parents did not use the Internet when researching vaccines even though they had Internet access.

Mergler et al.42

2002–2003, 2005

Quantitative, cross-sectional

1367 parents and 551 providers

CO, MA, MO, WA

C

Parents who agreed that a child's immune system could be weakened by too many immunizations or, conversely, who the community benefits from having children fully vaccinated; that the child benefited from vaccination; and that vaccines were very safe had greater odds of having a provider who shared those beliefs.

Omer et al.43

1993–2004

Quantitative, time-series cohort

4495 schools, 1111 cases

MI

S, E

A total of 23 significant clusters of high exemption rates and 6 clusters of pertussis cases were identified. There was a statistically significant geographic overlap between exemptions and pertussis case clusters. Census tracts in exemptions clusters were 3 times more likely to also be in a pertussis cluster than census tracts outside any exemptions cluster.

Omer et al.44

1991–2004; 1986–2004

Quantitative, time-series cohort

48 states, kindergarten or first-grade data

US, except MS and WV

S, E

States that easily granted exemptions had higher NME rates than states with medium and difficult exemption processes, as well as increased pertussis incidence. Although the mean exemption rate increased an average of 5% for easy-exemption-process states, there was no significant change in states with only religious exemptions or with medium or difficult exemption processes.

Omer et al.45

2005–2011

Quantitative, time-series cohort

50 states

US

S

Unadjusted rates of NME in states with easy exemption policies were 2.31 times as high as those of states with difficult exemption policies. By 2011, exemption rates in states with easy, medium, and hard exemption policies increased to 3.3%, 2.0%, and 1.3%, with annual rates of 13%, 18%, and 8%, respectively.

Peterson et al.46

February–May 2010

Quantitative, cross-sectional

2052 students in elementary, middle, and high schools in rural school district

WA

T

A total of 5.4% of children in kindergarten and 4.74% of children in kindergarten through 12th grade were exempted from immunizations, with higher exemptions in rural districts. Correcting school immunization records resulted in an increase in the number of students classified as fully immunized. After conducting school-based immunization clinics, the number of fully immunized students also increased.

Richards et al.47

1994–2009

Quantitative, time-series cohort

6392 schools

CA

T, C

The average school PBE rate increased from 0.6% in 1994 to 2.3% in 2009, an average of 9.2% per year. The average PBE rate among private schools was 1.77 times that among public schools, and its annual rate of increase was higher. Schools located in rural census tracts had 1.66 times higher PBE rates than those in urban census tracts. Exemption rates were also found to be associated with race, population density, education, and income.

Rota et al.48

January 1998

Mixed, cross-sectional survey

48 states, distributed to state health department immunization program managers

US, except MS and WV

S

Sixteen states delegated sole authority for processing exemptions to school officials, and 9 states had written policies informing parents who seek an exemption of the risks of not immunizing. The complexity of the exemption process was inversely associated with the proportion of exemptions filed.

Safi et al.8

2001–2010

Quantitative, time-series cohort

All students with exemptions in AR

AR

T, S

Exemptions increased steadily from 2003 after philosophical exemptions became allowed. Kindergarten had the steepest increase in exemptions. Medical exemptions declined by 55%, and religious exemptions declined and then increased. In the 2009–2010 school year, 70.8% of exemptions were requested for all vaccines, 9.2% were requested for ≥ 2 vaccines, and 20% were requested for a single vaccine. Of the single-vaccine exemptions, 93% were for the MMR and 4.6% were for HepB and varicella.

Salmon et al.49

1985–1992

Quantitative, time-series cohort

Mapping of exemptors by county in CA; individuals aged 5–19 y

US

E

On average, exemptors were 35 times more likely to contract measles; relative risk varied by age and year. When mapping exemptors by county in CA, exempt populations tended to be clustered in certain geographic regions. If the number of exemptors doubled, incidence of measles in nonexempt populations would increase by 5.5%, 18.6%, and 30.8%, respectively, for intergroup mixing ratios of 20%, 40%, and 60%.

Salmon et al.50

1998–2004

Quantitative, case-control

1367 parents, 391 of exempt children and 976 of fully vaccinated children

CO, MA, MO, WA

T, C, S

Most children (75%) with NMEs received at least some vaccines. Parents of exempt children were significantly more likely to report low perceived vaccine safety and efficacy, a low level of trust in the government, low perceived susceptibility to and severity of vaccine-prevented diseases, lower confidence in government sources for information, and higher confidence in alternative medicine professionals.

Salmon et al.51

May 2001– June 2002

Quantitative, cross-sectional

695 schools, surveys mailed to elementary school personnel who had completed state immunization report

CO, MA, MO, WA

C

Greater perceived disease susceptibility and severity of vaccines were associated with a decreased likelihood of a child in the school having an exemption. Children in schools at which the respondents were nurses or who had confidence in health departments were significantly less likely to be given an exemption. Use of professional organizations, government resources, and vaccine companies and pharmacists for vaccine information were associated with decreased likelihood of a child having an exemption.

Salmon et al.52

2001–2002

Quantitative, cross-sectional

1000 school immunization personnel in CO, MA, MO, and WA

CO, MA, MO, WA

S

School policies associated with an increased likelihood of children having exemptions included lack of provision of written instructions for completing the immunization requirement before enrollment, administrative procedures making it easier to claim an exemption, and granting of philosophical exemptions. A correlation was found between the number of procedures that make administration of exemptions difficult and a lower odds of actual exemptions.

Salmon et al.53

Not mentioned

Quantitative, case-control

780 parents

WI

T, C

Varicella vaccine and HepB vaccine were the top vaccines often not received by exempt children. The top reasons for seeking exemptions included the belief that vaccines might cause harm, that it was better to get natural disease, that the child was not at risk for disease, and that the child might develop autism. Exempt parents were also less likely to believe in disease susceptibility, severity, and vaccine efficacy and safety.

Smith et al.54

1995–2001

Quantitative, time-series cohort

151 720 children aged 19–35 mo, 795 of whom were unvaccinated

US

T, C, S

Undervaccinated children tended to be Black; have a younger mother who was not married and did not have a college degree; live in a poorer household; and live in a central city. Unvaccinated children tended to be White; have a mother who was married and had a college degree; live in a wealthier household; and have parents who expressed concerns regarding safety of vaccines. States that allowed philosophical exemptions also had significantly higher estimated rates of unvaccinated children.

Sugerman et al.55

2008

Mixed, discussion groups, survey, cross-sectional

839 patients

CA

T, C, E

PBE rates increased, and higher PBE rates in public schools were associated with higher median income. There was no significant effect of income in public charter and private schools. On the parent level, nearly all parents who reported declining or delaying vaccination were White and college educated. Most reported substantial skepticism of the government, pharmaceutical industry, and medical community; believed vaccination was unnecessary; and felt vaccines can produce a number of adverse health effects.

Thompson et al.56

2001–2002, 2002–2003, 2003–2004 school years

Quantitative, time-series cohort

Immunization exemptions granted for all AR school attendees, K–12

AR

T, S

Philosophical exemptions were found to be clustered geographically. After AR started allowing philosophical exemptions, the total number of exemptions granted increased by 23% from year 1 to year 2, by 17% from year 2 to year 3, and by 50% from year 3 to year 4. NMEs accounted for 79% of exemptions granted in years 1 and 2, 92% in year 3, and 95% in year 4.

Wenger et al.57

007

Mixed, cross-sectional

359 Amish parents

OH

T, C

A total of 68% stated that all of their children had received ≥ 1 immunization, and 17% reported that some of their children had received ≥ 1 immunization. Only 14% of the parents reported that none of their children had received immunizations. Reasons Amish parents resisted immunizations include concerns about adverse effects such as side effects, dangerous chemicals, and injection of a disease.

Note. NA = not available; NME = nonmedical exemption. Ellipses indicate that the state does not offer that particular exemption.Source. Centers for Disease Control and Prevention.26,28aThe philosophical and religious exemption rates were reported together for this state.

References

Authors and Disclosures

Authors and Disclosures

Eileen Wang is with the Department of the History and Sociology of Science, University of Pennsylvania, Philadelphia. Jessica Clymer is with the School of Nursing, University of Pennsylvania. Cecilia Davis-Hayes is with the Columbia University College of Physicians and Surgeons, New York, NY. Alison Buttenheim is with the School of Nursing, the Leonard Davis Institute, and the Center for Public Health Initiatives, University of Pennsylvania.

Correspondence should be sent to Alison Buttenheim, University of Pennsylvania School of Nursing, 235L Fagin Hall, 418 Curie Boulevard, Philadelphia, PA 19104 (e-mail: abutt@nursing.upenn.edu). Reprints can be ordered at http://www.ajph.org by clicking the "Reprints" link.